Pattern separation, completion, and categorisation in the hippocampus and neocortex
Abstract
The mechanisms for pattern completion and pattern separation are described in the context of a theory of hippocampal function in which the hippocampal CA3 system operates as a single attractor or autoassociation network to enable rapid, one-trial, associations between any spatial location (place in rodents, or spatial view in primates) and an object or reward, and to provide for completion of the whole memory during recall from any part. The factors important in the pattern completion in CA3 and also a large number of independent memories stored in CA3 include: a sparse distributed representation, representations that are independent due to the randomizing effect of the mossy fibres, heterosynaptic long-term depression as well as long-term potentiation in the recurrent collateral synapses, and diluted connectivity to minimize the number of multiple synapses between any pair of CA3 neurons which otherwise distort the basins of attraction. Recall of information from CA3 is implemented by the entorhinal cortex perforant path synapses to CA3 cells, which in acting as a pattern associator allow some pattern generalization. Pattern separation is performed in the dentate granule cells using competitive learning to convert grid-like entorhinal cortex firing to place-like fields, and in the dentate to CA3 connections that have diluted connectivity. Recall to the neocortex is achieved by a reverse hierarchical series of pattern association networks implemented by the hippocampo-cortical backprojections, each one of which performs some pattern generalization, to retrieve a complete pattern of cortical firing in higher-order cortical areas. New results on competitive networks show which factors contribute to their ability to perform pattern separation, pattern clustering, and pattern categorisation, and how these apply in different hippocampal and neocortical systems.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
This feature seems to depend on a pattern completion mechanism that is able to reinstate complete memories after partial cueing, based on the operation of hippocampal autoassociative neural networks.
“This feature seems to depend on a pattern completion mechanism that is able to reinstate complete memories after partial cueing, based on the operation of hippocampal autoassociative neural networks”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [81]
Cites
Neural networks and physical systems with emergent collective computational abilities.
Hopfield, J. J. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.8.2554 · Cited by 19,270 · see citing works
The magical number seven, plus or minus two: Some limits on our capacity for processing information.
Miller, G. A. (1956) · Psychological Review · doi:10.1037/h0043158 · Cited by 17,812 · see citing works
Plum, F. (1960) · Archives of Neurology · doi:10.1001/archneur.1960.03840090124020 · Cited by 10,388 · see citing works
Self-Organization and Associative Memory
Kohonen, T. (1989) · Springer Series in Information Sciences · doi:10.1007/978-3-642-88163-3 · Cited by 8,740 · see citing works
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
Introduction to the theory of neural computation
Hertz, J., Krogh, A., & Palmer, R. G. (1994) · Neural Networks · doi:10.1016/0893-6080(94)90014-0 · Cited by 6,431 · see citing works
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
Microstructure of a spatial map in the entorhinal cortex
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. (2005) · Nature · doi:10.1038/nature03721 · Cited by 4,068 · see citing works
Self-Organization and Associative Memory
Kohonen, T. (1988) · Springer series in information sciences · doi:10.1007/978-3-662-00784-6 · Cited by 3,825 · see citing works
Marr, D. (1969) · The Journal of Physiology · doi:10.1113/jphysiol.1969.sp008820 · Cited by 3,253 · see citing works
Reactivation of hippocampal ensemble memories during sleep
Wilson, M. A., & McNaughton, B. L. (1994) · Science · doi:10.1126/science.8036517 · Cited by 3,118 · see citing works
Faisal, A. A., Selen, L. P. J., & Wolpert, D. M. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2258 · Cited by 2,883 · see citing works
Simple memory: a theory for archicortex
Marr, D. (1971) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1971.0078 · Cited by 2,771 · see citing works
A theory of cerebellar function
Albus, J. S. (1971) · Mathematical Biosciences · doi:10.1016/0025-5564(71)90051-4 · Cited by 2,539 · see citing works
The Hippocampus as a Cognitive Map
Ranck, J. B. (1979) · American Journal of Psychiatry · doi:10.1176/ajp.136.10.1353 · Cited by 2,373 · see citing works
The cerebellum and neural control
Ito, M. (1984) · Cited by 2,314 · see citing works
Simplified neuron model as a principal component analyzer
Oja, E. (1982) · Journal of Mathematical Biology · doi:10.1007/bf00275687 · Cited by 2,309 · see citing works
Amit, D. J. (1989) · Cambridge University Press eBooks · doi:10.1017/cbo9780511623257 · Cited by 2,279 · see citing works
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
Dynamics of pattern formation in lateral-inhibition type neural fields
Амари, Ш.-И. (1977) · Biological Cybernetics · doi:10.1007/bf00337259 · Cited by 2,086 · see citing works
Path integration and the neural basis of the 'cognitive map'
McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., & Moser, M.-B. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1932 · Cited by 2,024 · see citing works
Long-Term Potentiation and Memory
Lynch, M. A. (2004) · Physiological Reviews · doi:10.1152/physrev.00014.2003 · Cited by 2,001 · see citing works
The cerebellum and neural control
Tindall, S. C. (1985) · Surgical Neurology · doi:10.1016/0090-3019(85)90320-9 · Cited by 1,760 · see citing works
A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation
Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L. M., Barker, R. A., Gage, F. H., et al. (2009) · Science · doi:10.1126/science.1173215 · Cited by 1,642 · see citing works
Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus
Leutgeb, J. K., Leutgeb, S., Moser, M.-B., & Moser, E. I. (2007) · Science · doi:10.1126/science.1135801 · Cited by 1,601 · cited 6× · see citing works
“Pattern separation and the sparseness of the firing of the dentate granule cell input via the mossy fibres to CA3 cells The firing activity of dentate granule cells appears to be very sparse (Jung & McNaughton, 1993; Leutgeb et al., 2007) and this, together with the small number of dentate mossy fibre connections on e…”
BackgroundInfluentialCellular networks underlying human spatial navigation
Ekstrom, A. D., Kahana, M. J., Caplan, J. B., Fields, T. A., Isham, E. A., Newman, E. L., & Fried, I. (2003) · Nature · doi:10.1038/nature01964 · Cited by 1,425 · see citing works
Spatial representation in the entorhinal cortex
Fyhn, M., Molden, S., Witter, M. P., Moser, E. I., & Moser, M.-B. (2004) · Science · doi:10.1126/science.1099901 · Cited by 1,339 · see citing works
Hippocampal synaptic enhancement and information storage within a distributed memory system
McNaughton, B. L., & Morris, R. G. M. (1987) · Trends in Neurosciences · doi:10.1016/0166-2236(87)90011-7 · Cited by 1,304 · see citing works
Internally Generated Cell Assembly Sequences in the Rat Hippocampus
Pastalkova, E., Itskov, V., Amarasingham, A., & Buzsáki, G. (2008) · Science · doi:10.1126/science.1159775 · Cited by 1,301 · see citing works
Computational analysis of the role of the hippocampus in memory
Treves, A., & Rolls, E. T. (1994) · Hippocampus · doi:10.1002/hipo.450040319 · Cited by 1,272 · see citing works
Self-citationProbabilistic decision making by slow reverberation in cortical circuits
Wang, X.-J. (2002) · Neuron · doi:10.1016/s0896-6273(02)01092-9 · Cited by 1,242 · see citing works
Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys
Carmichael, S. T., & Price, J. L. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903630408 · Cited by 1,197 · see citing works
Hippocampal ‘time cells’ bridge the gap in memory for discontiguous events
MacDonald, C. J., Lepage, K. Q., Eden, U. T., & Eichenbaum, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.012 · Cited by 1,193 · see citing works
(2006) · doi:10.1093/acprof:oso/9780195100273.001.0001 · Cited by 1,186 · see citing works
Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents
Suzuki, W., & Amaral, D. G. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903500402 · Cited by 1,134 · see citing works
Parallel models of associative memory
Heath, R. A. (1982) · Journal of Mathematical Psychology · doi:10.1016/0022-2496(82)90036-0 · Cited by 1,111 · see citing works
Requirement for Hippocampal CA3 NMDA Receptors in Associative Memory Recall
Nakazawa, K., Quirk, M. C., Chitwood, R. A., Watanabe, M., Yeckel, M. F., Sun, L. D., Kato, A., Carr, C. A., Johnston, D., Wilson, M. A., et al. (2002) · Science · doi:10.1126/science.1071795 · Cited by 1,090 · see citing works
McNaughton, B. L., Barnes, C. A., & O'Keefe, J. (1983) · Experimental Brain Research · doi:10.1007/bf00237147 · Cited by 1,071 · see citing works
Amit, D. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.3.237 · Cited by 1,061 · see citing works
Zhang, K. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-02112.1996 · Cited by 1,001 · see citing works
Path integration and cognitive mapping in a continuous attractor neural network model
Samsonovich, A., & McNaughton, B. L. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-15-05900.1997 · Cited by 989 · see citing works
Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network
McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., Lowell, B. B., Fanselow, M. S., Wilson, M. A., & Tonegawa, S. (2007) · Science · doi:10.1126/science.1140263 · Cited by 958 · see citing works
Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade‐off
O'Reilly, R. C., & McClelland, J. L. (1994) · Hippocampus · doi:10.1002/hipo.450040605 · Cited by 914 · see citing works
Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat
Ishizuka, N., Weber, J., & Amaral, D. G. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902950407 · Cited by 899 · see citing works
Moscovitch, M., Rosenbaum, R. S., Gilboa, A., Addis, D. R., Westmacott, R., Grady, C., McAndrews, M. P., Levine, B., Black, S., Winocur, G., et al. (2005) · Journal of Anatomy · doi:10.1111/j.1469-7580.2005.00421.x · Cited by 893 · see citing works
Neural Networks and Brain Function
Rolls, E. T., & Treves, A. (1997) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198524328.001.0001 · Cited by 885 · see citing works
Self-citationCerebellar circuitry as a neuronal machine
Ito, M. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.02.006 · Cited by 880 · see citing works
Nakashiba, T., Cushman, J. D., Pelkey, K. A., Renaudineau, S., Buhl, D. L., McHugh, T. J., Barrera, V. R., Chittajallu, R., Iwamoto, K. S., McBain, C. J., et al. (2012) · Cell · doi:10.1016/j.cell.2012.01.046 · Cited by 805 · see citing works
Spatial selectivity of unit activity in the hippocampal granular layer
Jung, M. W., & McNaughton, B. L. (1993) · Hippocampus · doi:10.1002/hipo.450030209 · Cited by 789 · see citing works
Single unit activity in the rat hippocampus during a spatial memory task
O'Keefe, J. M., & Speakman, A. (1987) · Experimental Brain Research · doi:10.1007/bf00255230 · Cited by 782 · see citing works
Accurate Path Integration in Continuous Attractor Network Models of Grid Cells
Burak, Y., & Fiete, I. R. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000291 · Cited by 779 · see citing works
Anatomy of hierarchy: Feedforward and feedback pathways in macaque visual cortex
Markov, N. T., Vezoli, J., Chameau, P., Falchier, A., Quilodran, R., Huissoud, C., Lamy, C., Misery, P., Giroud, P., Ullman, S., et al. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23458 · Cited by 759 · see citing works
GABAergic Cells Are the Major Postsynaptic Targets of Mossy Fibers in the Rat Hippocampus
Acsády, L., Kamondi, A., Sı́k, A., Freund, T., & Buzsáki, G. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03386.1998 · Cited by 741 · see citing works
Chaotic Balanced State in a Model of Cortical Circuits
van Vreeswijk, C., & Sompolinsky, H. (1998) · Neural Computation · doi:10.1162/089976698300017214 · Cited by 711 · see citing works
Treves, A., & Rolls, E. T. (1992) · Hippocampus · doi:10.1002/hipo.450020209 · Cited by 702 · see citing works
Self-citationAn oscillatory interference model of grid cell firing
Burgess, N., Barry, C., & O'Keefe, J. M. (2007) · Hippocampus · doi:10.1002/hipo.20327 · Cited by 688 · see citing works
Attractor Dynamics in the Hippocampal Representation of the Local Environment
Wills, T. J., Lever, C., Cacucci, F., Burgess, N., & O'Keefe, J. M. (2005) · Science · doi:10.1126/science.1108905 · Cited by 643 · see citing works
Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1
Gilbert, P. E., Kesner, R. P., & Lee, I. (2001) · Hippocampus · doi:10.1002/hipo.1077 · Cited by 641 · see citing works
A Spin Glass Model of Path Integration in Rat Medial Entorhinal Cortex
Fuhs, M. C., & Touretzky, D. S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4353-05.2006 · Cited by 628 · see citing works
The parahippocampal gyrus: New observations regarding its cortical connections in the monkey
Hoesen, G. W. V. (1982) · Trends in Neurosciences · doi:10.1016/0166-2236(82)90201-6 · Cited by 624 · see citing works
NMDA receptors, place cells and hippocampal spatial memory
Nakazawa, K., McHugh, T. J., Wilson, M. A., & Tonegawa, S. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1385 · Cited by 619 · see citing works
A computational theory of hippocampal function, and empirical tests of the theory
Rolls, E. T., & Kesner, R. P. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.04.005 · Cited by 608 · see citing works
Self-citationPlace cells and place recognition maintained by direct entorhinal-hippocampal circuitry
Brun, V. H., Otnæss, M. K., Molden, S., Steffenach, H.-A., Witter, M. P., Moser, M.-B., & Moser, E. I. (2002) · Science · doi:10.1126/science.1071089 · Cited by 606 · see citing works
Suzuki, W., & Amaral, D. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-03-01856.1994 · Cited by 587 · see citing works
Central olfactory connections in the macaque monkey
Carmichael, S. T., Clugnet, M.-C., & Price, J. L. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903460306 · Cited by 578 · see citing works
Hebbian synapses: biophysical mechanisms and algorithms.
Brown, T. H., Kairiss, E. W., & Keenan, C. L. (1990) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.13.030190.002355 · Cited by 577 · see citing works
A review of the hippocampal place cells
O'Keefe, J. M. (1979) · Progress in Neurobiology · doi:10.1016/0301-0082(79)90005-4 · Cited by 569 · see citing works
Anatomical organization of the parahippocampal-hippocampal network
WITTER, M. P., WOUTERLOOD, F. G., NABER, P. A., & VAN HAEFTEN, T. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06716.x · Cited by 567 · see citing works
Computational Neuroscience of Vision
Rolls, E. T., & Deco, G. (2001) · doi:10.1093/acprof:oso/9780198524885.001.0001 · Cited by 551 · see citing works
Self-citationPlace Cells, Grid Cells, and MemoryPreprint
Moser, M., Rowland, D. C., & Moser, E. I. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021808 · Cited by 538 · see citing works
Hippocampal-Neocortical Interactions in Memory Formation, Consolidation, and Reconsolidation
Wang, S., & Morris, R. (2009) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100523 · Cited by 536 · see citing works
Organization of the entorhinal—hippocampal system: A review of current anatomical data
Witter, M. P. (1993) · Hippocampus · doi:10.1002/hipo.1993.4500030707 · Cited by 534 · see citing works
Temporal association in asymmetric neural networks.
Sompolinsky, H., & Kanter, I. (1986) · Physical Review Letters · doi:10.1103/physrevlett.57.2861 · Cited by 531 · see citing works
Hippocampal “Time Cells”: Time versus Path Integration
Kraus, B. J., Robinson, R. J., White, J. A., Eichenbaum, H., & Hasselmo, M. E. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.015 · Cited by 526 · see citing works
Chapter 1 Chapter Neurons, numbers and the hippocampal network
Amaral, D. G., Ishizuka, N., & Claiborne, B. J. (1990) · Progress in brain research · doi:10.1016/s0079-6123(08)61237-6 · Cited by 523 · see citing works
Hippocampal CA3 NMDA Receptors Are Crucial for Memory Acquisition of One-Time Experience
Nakazawa, K., Sun, L. D., Quirk, M. C., Rondi‐Reig, L., Wilson, M. A., & Tonegawa, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00165-x · Cited by 506 · see citing works
Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo
Henze, D. A., Wittner, L., & Buzsáki, G. (2002) · Nature Neuroscience · doi:10.1038/nn887 · Cited by 480 · see citing works
Morris, R., Moser, E. I., Riedel, G., Martin, S. J., Sandin, J., Day, M., & O’Carroll, C. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1264 · Cited by 480 · see citing works
A map of visual space in the primate entorhinal cortex
Killian, N. J., Jutras, M. J., & Buffalo, E. A. (2012) · Nature · doi:10.1038/nature11587 · Cited by 471 · see citing works
Hasselmo, M. E., Schnell, E., & Barkai, E. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-05249.1995 · Cited by 463 · see citing works
Neunuebel, J. P., & Knierim, J. J. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.017 · Cited by 454 · see citing works
Emotion and Decision-making Explained
Rolls, E. T. (2013) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199659890.001.0001 · Cited by 445 · see citing works
Self-citationLimbic systems for emotion and for memory, but no single limbic system
Rolls, E. T. (2013) · Cortex · doi:10.1016/j.cortex.2013.12.005 · Cited by 428 · see citing works
Self-citationParallel Distributed Processing: Implications for Psychology and Neurobiology
Wolters, G. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90131-s · Cited by 418 · see citing works
Associative memory. A system-theoretical approach
(1979) · Acta Biotheoretica · doi:10.1007/bf00054681 · Cited by 400 · see citing works
Neurobiology of comparative cognition
Walker, S. F. (1991) · Biological Psychology · doi:10.1016/0301-0511(91)90020-h · Cited by 398 · see citing works
Theta-paced flickering between place-cell maps in the hippocampus
Jezek, K., Henriksen, E. J., Treves, A., Moser, E. I., & Moser, M.-B. (2011) · Nature · doi:10.1038/nature10439 · Cited by 359 · see citing works
Kumaran, D., & McClelland, J. L. (2012) · Psychological Review · doi:10.1037/a0028681 · Cited by 358 · see citing works
What determines the capacity of autoassociative memories in the brain?
Treves, A., & Rolls, E. T. (1991) · Network Computation in Neural Systems · doi:10.1088/0954-898x_2_4_004 · Cited by 354 · see citing works
Self-citationEnsemble Dynamics of Hippocampal Regions CA3 and CA1
Guzowski, J. F., Knierim, J. J., & Moser, E. I. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.003 · Cited by 354 · see citing works
A computational theory of hippocampal function, and tests of the theory: New developments
Kesner, R. P., & Rolls, E. T. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.009 · Cited by 347 · see citing works
Self-citationBehavioral functions of the CA3 subregion of the hippocampusPreprint
Kesner, R. P. (2007) · Learning & Memory · doi:10.1101/lm.688207 · Cited by 337 · see citing works
Hasselmo, M. E., & Wyble, B. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00048-x · Cited by 337 · see citing works
Neuroscience and Connectionist Theory
Gluck, M. A., & Rumelhart, D. E. (2013) · Psychology Press eBooks · doi:10.4324/9780203762981 · Cited by 320 · see citing works
The role of the hippocampus in memory for the temporal order of a sequence of odors.
Kesner, R. P., Gilbert, P. E., & Barua, L. A. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.2.286 · Cited by 309 · see citing works
Imaging memory in temporal lobe epilepsy: predicting the effects of temporal lobe resection
Bonelli, S. B., Powell, R., Yogarajah, M., Samson, R. S., Symms, M. R., Thompson, P. J., Koepp, M. J., & Duncan, J. S. (2010) · Brain · doi:10.1093/brain/awq006 · Cited by 295 · see citing works
Functions of Neuronal Networks in the Hippocampus and Neocortex in Memory
Rolls, E. T. (1989) · Elsevier eBooks · doi:10.1016/b978-0-12-148955-7.50017-5 · Cited by 292 · see citing works
Self-citationThe Noisy BrainStochastic Dynamics as a Principle of Brain Function
Rolls, E. T., & Deco, G. (2010) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199587865.001.0001 · Cited by 289 · see citing works
Self-citationPrediction, sequences and the hippocampus
Lisman, J. E., & Redish, A. D. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0316 · Cited by 285 · see citing works
The neuronal encoding of information in the brain
Rolls, E. T., & Treves, A. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.08.002 · Cited by 284 · see citing works
Self-citationHunsaker, M. R., & Kesner, R. P. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.09.014 · Cited by 283 · see citing works
A computational theory of episodic memory formation in the hippocampus
Rolls, E. T. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.03.027 · Cited by 271 · see citing works
Self-citationMemory: Anatomical Organization of Candidate Brain Regions
Amaral, D. G. (1987) · Comprehensive physiology · doi:10.1002/cphy.cp010507 · Cited by 262 · see citing works
Theta rhythm and the encoding and retrieval of space and time
Hasselmo, M. E., & Stern, C. E. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.06.022 · Cited by 261 · see citing works
The role of the hippocampus in memory for the temporal order of a sequence of odors.
Kesner, R. P., Gilbert, P. E., & Barua, L. A. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.2.286 · Cited by 261 · see citing works
Glutamate-receptor-mediated encoding and retrieval of paired-associate learning
Day, M., Langston, R. F., & Morris, R. (2003) · Nature · doi:10.1038/nature01769 · Cited by 259 · see citing works
Naber, P. A., da Silva, F. H. L., & Witter, M. P. (2001) · Hippocampus · doi:10.1002/hipo.1028 · Cited by 258 · see citing works
The emergence of grid cells: Intelligent design or just adaptation?
Kropff, E., & Treves, A. (2008) · Hippocampus · doi:10.1002/hipo.20520 · Cited by 254 · see citing works
Lee, I., & Kesner, R. P. (2004) · Hippocampus · doi:10.1002/hipo.10167 · Cited by 253 · see citing works
Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning
Rolls, E. T., Stringer, S. M., & Elliot, T. (2006) · Network Computation in Neural Systems · doi:10.1080/09548980601064846 · Cited by 250 · see citing works
Self-citationEmerging principles of intrinsic hippocampal organization
Amaral, D. G. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90214-j · Cited by 249 · see citing works
Hebb-Marr Networks and the Neurobiological Representation of Action in Space
Gluck, M. A., & Rumelhart, D. E. (2013) · Psychology Press eBooks · doi:10.4324/9780203762981-6 · Cited by 246 · see citing works
A computational principle for hippocampal learning and neurogenesis
Becker, S. (2005) · Hippocampus · doi:10.1002/hipo.20095 · Cited by 244 · see citing works
Spatial View Cells in the Primate Hippocampus
Rolls, E. T., Robertson, R. G., & Georges‐François, P. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01538.x · Cited by 242 · see citing works
Self-citationNeuronal computations underlying the firing of place cells and their role in navigation
Burgess, N., & O'Keefe, J. M. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:6 · Cited by 240 · see citing works
Intrinsic and extrinsic wiring of CA3: Indications for connectional heterogeneityPreprint
Witter, M. P. (2007) · Learning & Memory · doi:10.1101/lm.725207 · Cited by 234 · see citing works
Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map
Leutgeb, S., & Leutgeb, J. K. (2007) · Learning & Memory · doi:10.1101/lm.703907 · Cited by 234 · see citing works
The Oxford Handbook of Comparative Cognition
(2012) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780195392661.001.0001 · Cited by 232 · see citing works
Long-term potentiation and memory
Morris, R. G. M. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1230 · Cited by 232 · see citing works
Computational Models of Grid Cells
Giocomo, L. M., Moser, M., & Moser, E. I. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.023 · Cited by 231 · see citing works
A Computational Approach to Hippocampal Function
Levy, W. B. (1989) · The Psychology of learning and motivation/The psychology of learning and motivation · doi:10.1016/s0079-7421(08)60113-9 · Cited by 228 · see citing works
Georges‐François, P. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.3.197 · Cited by 226 · see citing works
Lassalle, J., Bataille, T., & Halley, H. (2000) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1999.3931 · Cited by 213 · see citing works
Rolls, E. T., & Treves, A. (1990) · Network Computation in Neural Systems · doi:10.1088/0954-898x_1_4_002 · Cited by 208 · see citing works
Self-citationMemory, Attention, and Decision-Making: A unifying computational neuroscience approach
Rolls, E. T. (2007) · Cited by 205 · see citing works
Self-citationStefanacci, L., Suzuki, W., & Amaral, D. G. (1996) · The Journal of comparative neurology · doi:10.1002/(sici)1096-9861(19961125)375:4 · Cited by 199 · see citing works
The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat
Gold, A., & Kesner, R. P. (2005) · Hippocampus · doi:10.1002/hipo.20103 · Cited by 196 · see citing works
Brain mechanisms for perceptual and reward-related decision-making
Deco, G., Rolls, E. T., Albantakis, L., & Romo, R. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.01.010 · Cited by 196 · see citing works
Self-citationA Unified Mathematical Framework for Coding Time, Space, and Sequences in the Hippocampal Region
Howard, M. W., MacDonald, C. J., Tiganj, Z., Shankar, K. H., Du, Q., Hasselmo, M. E., & Eichenbaum, H. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5808-12.2014 · Cited by 195 · see citing works
Goodrich‐Hunsaker, N. J., Hunsaker, M. R., & Kesner, R. P. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.1.16 · Cited by 194 · see citing works
Battaglia, F. P., & Treves, A. (1998) · Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics · doi:10.1103/physreve.58.7738 · Cited by 194 · see citing works
Attention and working memory: a dynamical model of neuronal activity in the prefrontal cortex
Deco, G., & Rolls, E. T. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02956.x · Cited by 187 · see citing works
Self-citationCerebral cortex : principles of operation
Rolls, E. T. (2016) · doi:10.82444/warw.33712699 · Cited by 187 · see citing works
Self-citationDecision‐making and Weber's law: a neurophysiological model
Deco, G., & Rolls, E. T. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04940.x · Cited by 179 · see citing works
Self-citationInformation About Spatial View in an Ensemble of Primate Hippocampal Cells
Rolls, E. T., Treves, A., Robertson, R. G., Georges‐François, P., & Panzeri, S. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.4.1797 · Cited by 179 · see citing works
Self-citationA Specific Role of the Human Hippocampus in Recall of Temporal Sequences
Lehn, H., Steffenach, H.-A., van Strien, N. M., Veltman, D. J., Witter, M. P., & Haberg, A. K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5370-08.2009 · Cited by 176 · see citing works
Neural 'bubble' dynamics in two dimensions: foundations
Taylor, J. G. (1999) · Biological Cybernetics · doi:10.1007/s004220050534 · Cited by 172 · see citing works
Invariant Visual Object and Face Recognition: Neural and Computational Bases, and a Model, VisNet
Rolls, E. T. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00035 · Cited by 169 · see citing works
Self-citationGiocomo, L. M., & Hasselmo, M. E. (2007) · Molecular Neurobiology · doi:10.1007/s12035-007-0032-z · Cited by 161 · see citing works
Sidhu, M. K., Stretton, J., Winston, G. P., Bonelli, S. B., Centeno, M., Vollmar, C., Symms, M. R., Thompson, P. J., Koepp, M. J., & Duncan, J. S. (2013) · Brain · doi:10.1093/brain/awt099 · Cited by 158 · see citing works
A model of episodic memory: Mental time travel along encoded trajectories using grid cells
Hasselmo, M. E. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.07.005 · Cited by 157 · see citing works
Role of CA3 and CA1 subregions of the dorsal hippocampus on temporal processing of objects
Hoge, J., & Kesner, R. P. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.04.013 · Cited by 156 · see citing works
Spatial View Cells in the Primate Hippocampus: Effects of Removal of View Details
Robertson, R. G., Rolls, E. T., & Georges‐François, P. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.3.1145 · Cited by 153 · see citing works
Self-citationKleinfeld, D., & Sompolinsky, H. (1988) · Biophysical Journal · doi:10.1016/s0006-3495(88)83041-8 · Cited by 150 · see citing works
Graded-response neurons and information encodings in autoassociative memories
Treves, A. (1990) · Physical Review A · doi:10.1103/physreva.42.2418 · Cited by 149 · see citing works
An analysis of the dentate gyrus function
Kesner, R. P. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.01.012 · Cited by 148 · see citing works
Attractor neural network models of spatial maps in hippocampus
Tsodyks, M. V. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:4 · Cited by 147 · see citing works
Self-citationGilbert, P. E., & Kesner, R. P. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.6.1385 · Cited by 146 · see citing works
Object, Space, and Object-Space Representations in the Primate Hippocampus
Rolls, E. T., Xiang, J.-Z., & Franco, L. (2005) · Journal of Neurophysiology · doi:10.1152/jn.01063.2004 · Cited by 145 · see citing works
Self-citationStringer, S. M., Trappenberg, T. P., Rolls, E. T., & de Araújo, I. E. (2002) · Network Computation in Neural Systems · doi:10.1088/0954-898x/13/2/304 · Cited by 144 · see citing works
Self-citationMemory Deficits Characterized by Patterns of Lesions to the Hippocampus and Parahippocampal Cortex
Bohbot, V. D., Allen, J. J. B., & Nadel, L. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06737.x · Cited by 140 · see citing works
Neural models of plasticity: experimental and theoretical approaches
Byrne, J. H., & Berry, W. O. (1990) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(90)90284-y · Cited by 140 · see citing works
Florian, C., & Roullet, P. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.03.003 · Cited by 139 · see citing works
van Haeften, T., Baks‐te‐Bulte, L., Goede, P. H., Wouterlood, F. G., & Witter, M. P. (2003) · Hippocampus · doi:10.1002/hipo.10144 · Cited by 136 · see citing works
Per, A., Morris, R., David, A., Tim, B., & O'Keefe, J. M. (2006) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195100273.003.0001 · Cited by 135 · see citing works
Hunsaker, M. R., & Kesner, R. P. (2008) · Hippocampus · doi:10.1002/hipo.20455 · Cited by 133 · see citing works
Rolls, E. T. (1989) · Addison-Wesley Longman Publishing Co., Inc. eBooks · Cited by 132 · see citing works
Self-citationAn assessment of Marr’s theory of the hippocampus as a temporary memory store
Willshaw, D. J., & Buckingham, J. T. (1990) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1990.0165 · Cited by 130 · see citing works
Reward-Spatial View Representations and Learning in the Primate Hippocampus
Rolls, E. T., & Xiang, J.-Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1481-05.2005 · Cited by 129 · see citing works
Self-citationAssociative memory: A system-theoretical approach
Whitehead, B. A. (1977) · Mathematical Biosciences · doi:10.1016/0025-5564(77)90055-4 · Cited by 126 · see citing works
The recall of events through the learning of associations between their parts
Gardner-Medwin, A. R. (1976) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1976.0084 · Cited by 125 · see citing works
The neural and molecular bases of learning
Bruyn, G. W. (1987) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(87)90195-x · Cited by 123 · see citing works
Lavenex, P., SUZUKI, W. A., & Amaral, D. G. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20079 · Cited by 122 · see citing works
A quantitative theory of the functions of the hippocampal CA3 network in memory
Rolls, E. T. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00098 · Cited by 122 · see citing works
Self-citationStringer, S. M., Trappenberg, T. P., Rolls, E. T., & de Araújo, I. E. (2002) · Network Computation in Neural Systems · doi:10.1080/net.13.2.217.242 · Cited by 119 · see citing works
Self-citationThe Noisy Brain: Stochastic Dynamics as a Principle of Brain Function
Dawkins, M. S. (2010) · Animal Behaviour · doi:10.1016/j.anbehav.2010.04.019 · Cited by 118 · see citing works
Merrill, D. A., Chiba, A. A., & Tuszynski, M. H. (2001) · Journal of Comparative Neurology · doi:10.1002/cne.1327 · Cited by 118 · see citing works
Delatour, B., & Witter, M. P. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01973.x · Cited by 117 · see citing works
Pitkänen, A., Kelly, J. L., & Amaral, D. G. (2002) · Hippocampus · doi:10.1002/hipo.1099 · Cited by 109 · see citing works
Spatial View Cells in the Primate Hippocampus and Memory Recall
Rolls, E. T., & Xiang, J.-Z. (2006) · Reviews in the Neurosciences · doi:10.1515/revneuro.2006.17.1-2.175 · Cited by 108 · see citing works
Self-citationStringer, S. M., Rolls, E. T., Trappenberg, T. P., & de Araújo, I. E. (2002) · Network Computation in Neural Systems · doi:10.1088/0954-898x_13_4_301 · Cited by 106 · see citing works
Self-citationModels of Grid Cell Spatial Firing Published 2005–2011
Zilli, E. A. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00016 · Cited by 105 · see citing works
The Role of CA3 Hippocampal NMDA Receptors in Paired Associate Learning
Rajji, T. K., Chapman, D. E., Eichenbaum, H., & Greene, R. W. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4194-05.2006 · Cited by 105 · see citing works
Hippocampal–cortical interactions and the dynamics of memory trace reactivation
Schwindel, C. D., & McNaughton, B. L. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53839-0.00011-9 · Cited by 101 · see citing works
Evaluating the temporal context of episodic memory: The role of CA3 and CA1
Hunsaker, M. R. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.11.015 · Cited by 101 · see citing works
Kesner, R. P., Hunsaker, M. R., & Warthen, M. W. (2008) · Behavioral Neuroscience · doi:10.1037/a0013592 · Cited by 100 · see citing works
Invariant Object Recognition in the Visual System with Novel Views of 3D Objects
Stringer, S. M., & Rolls, E. T. (2002) · Neural Computation · doi:10.1162/089976602760407982 · Cited by 97 · see citing works
Self-citation(2008) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(08)x0003-7 · Cited by 97 · see citing works
Role of long‐term synaptic modification in short‐term memory
Kesner, R. P., & Rolls, E. T. (2001) · Hippocampus · doi:10.1002/hipo.1040 · Cited by 94 · see citing works
Self-citationInformation Theory and the Brain
Baddeley, R. (2000) · Cambridge University Press eBooks · doi:10.1017/cbo9780511665516 · Cited by 93 · see citing works
Genetic neuroscience of mammalian learning and memory
Tonegawa, S., Nakazawa, K., & Wilson, M. A. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1243 · Cited by 93 · see citing works
Computational Models of Learning in Simple Neural Systems
(1989) · The Psychology of learning and motivation/The psychology of learning and motivation · doi:10.1016/s0079-7421(08)x6009-8 · Cited by 93 · see citing works
Long-Term Potentiation in Two Synaptic Systems of the Hippocampal Brain Slice
Brown, T. H., Ganong, A. H., Kairiss, E. W., Keenan, C. L., & Kelso, S. R. (1989) · Elsevier eBooks · doi:10.1016/b978-0-12-148955-7.50018-7 · Cited by 92 · see citing works
Rondi‐Reig, L., Libbey, M., Eichenbaum, H., & Tonegawa, S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.041620798 · Cited by 92 · see citing works
A unified model of spatial and episodic memory
Rolls, E. T., Stringer, S. M., & Trappenberg, T. P. (2002) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.2009 · Cited by 91 · see citing works
Self-citationSimulation studies of the CA3 hippocampal subfield modelled as an attractor neural network
Rolls, E. T., Treves, A., Foster, D. J., & Pérez-Vicente, C. (1997) · Neural Networks · doi:10.1016/s0893-6080(97)00092-0 · Cited by 91 · see citing works
Self-citationNeuronal selectivity, population sparseness, and ergodicity in the inferior temporal visual cortex
Franco, L., Rolls, E. T., Aggelopoulos, N. C., & Jerez, J. M. (2007) · Biological Cybernetics · doi:10.1007/s00422-007-0149-1 · Cited by 90 · see citing works
Self-citationMiller, P. C., & Wang, X. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508072103 · Cited by 88 · see citing works
The CRISP theory of hippocampal function in episodic memory
Cheng, S. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00088 · Cited by 87 · see citing works
Open Peer Review by a Selected-Papers Network
Lee, C. J. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00001 · Cited by 85 · see citing works
Rolls, E. T. (2009) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1 · Cited by 81 · see citing works
Self-citationIntrinsic connections of the macaque monkey hippocampal formation: II. CA3 connections
Kondo, H., Lavenex, P., & Amaral, D. G. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22056 · Cited by 79 · see citing works
Quantitative estimate of the information relayed by the Schaffer collaterals
Treves, A. (1995) · Journal of Computational Neuroscience · doi:10.1007/bf00961437 · Cited by 77 · see citing works
Stringer, S. M., Rolls, E. T., & Trappenberg, T. P. (2003) · Neural Networks · doi:10.1016/s0893-6080(03)00210-7 · Cited by 71 · see citing works
Self-citationOn the design of neural networks in the brain by genetic evolution
Rolls, E. T., & Stringer, S. M. (2000) · Progress in Neurobiology · doi:10.1016/s0301-0082(99)00066-0 · Cited by 69 · see citing works
Self-citationFunctions of the primate hippocampus in spatial and nonspatial memory
Rolls, E. T. (1991) · Hippocampus · doi:10.1002/hipo.450010310 · Cited by 66 · see citing works
Self-citationde Araújo, I. E., Rolls, E. T., & Stringer, S. M. (2001) · Hippocampus · doi:10.1002/hipo.1085 · Cited by 62 · see citing works
Self-citationSelf-organizing continuous attractor network models of hippocampal spatial view cells
Stringer, S. M., Rolls, E. T., & Trappenberg, T. P. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.08.003 · Cited by 57 · see citing works
Self-citationTheoretical and Neurophysiological Analysis of the Functions of the Primate Hippocampus in MemoryPreprint
Rolls, E. T. (1990) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1990.055.01.095 · Cited by 57 · see citing works
Self-citationHow Informative Are Spatial CA3 Representations Established by the Dentate Gyrus?
Cerasti, E., & Treves, A. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000759 · Cited by 54 · see citing works
Flagged first, then by citations
3 of the 227 references couldn’t be matched to a known paper.
Research works printed but not linked: 3
- McNaughton, 1991, Associative pattern completion in hippocampal circuits: New evidence and new questions, Brain Research Reviews, 16, 193
- Rolls, 1995, A model of the operation of the hippocampus and entorhinal cortex in memory, International Journal of Neural Systems, 6, 51
- Witter, 2000, Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways, Hippocampus, 10, 398, 10.1002/1098-1063(2000)10:4<398::aid-hipo6>3.0.co;2-k · DOI
Cited by
Sorted by citations
Roddy, D. W., Farrell, C., Doolin, K., Roman, E., Tozzi, L., Frodl, T., O’Keane, V., & O’Hanlon, E. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.08.021 · Cited by 287 · see citing works
The enigmatic mossy cell of the dentate gyrus
Scharfman, H. E. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.87 · Cited by 290 · see citing works
Re-evaluating Circuit Mechanisms Underlying Pattern Separation
Cayco-Gajic, N. A., & Silver, R. A. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.044 · Cited by 220 · see citing works
“As the first stage in this pathway, the dentate gyrus is thought to separate entorhinal input patterns prior to memory storage in the hippocampus (Marr, 1971; McNaughton and Morris, 1987; Yassa and Stark, 2011; Schmidt et al., 2012; Knierim and Neunuebel, 2016; Rolls, 2016).”
Cerebral cortex : principles of operation
Rolls, E. T. (2016) · doi:10.82444/warw.33712699 · Cited by 187 · see citing works
Self-citationThe storage and recall of memories in the hippocampo-cortical system
Rolls, E. T. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2744-3 · Cited by 183 · see citing works
“For recall, the hippocampal output can be thought of as a pointer to neocortical neurons via which memories can be called by using the backprojection pathways (Kesner and Rolls 2015; Rolls 2016a).”
BackgroundMethodResultInfluentialSelf-citationEspinoza, C., Guzman, S. J., Zhang, X., & Jónás, P. (2018) · Nature Communications · doi:10.1038/s41467-018-06899-3 · Cited by 178 · see citing works
Hippocampal Maturation Drives Memory from Generalization to Specificity
Keresztes, A., Ngo, C. T., Lindenberger, U., Werkle‐Bergner, M., & Newcombe, N. S. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.05.004 · Cited by 170 · see citing works
The Human Dentate Gyrus Plays a Necessary Role in Discriminating New Memories
Baker, S., Vieweg, P., Gao, F., Gilboa, A., Wolbers, T., Black, S. E., & Rosenbaum, R. S. (2016) · Current Biology · doi:10.1016/j.cub.2016.07.081 · Cited by 148 · see citing works
The neurobiology of human fear generalization: meta-analysis and working neural model
Webler, R. D., Berg, H. E., Fhong, K., Tuominen, L. J., Holt, D. J., Morey, R. A., Lange, I., Burton, P. C., Fullana, M. A., Raduà, J., et al. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.035 · Cited by 148 · see citing works
“Importantly, the LC-CA3 and BA-CA1 pathways earlier triggered by rapid low-road processing of the GS, are R.D. Webler et al. Neuroscience and Biobehavioral Reviews 128 (2021) 421–436 proposed to increase the neural gain in CA3/CA1-based pattern completion circuits with the effect of predisposing the hippocampus toward…”
InfluentialThe hippocampus, ventromedial prefrontal cortex, and episodic and semantic memory
Rolls, E. T. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102334 · Cited by 144 · see citing works
“…with each other) receive taste, somatosensory, olfactory, visual, and auditory inputs that are needed to build the reward and punishment value representations that are found in these regions but much less in the preceding cortical areas that provide these inputs (Rolls, 2016a, 2019a, 2019c, 2021a).”
BackgroundInfluentialSelf-citationAge-related deficits in the mnemonic similarity task for objects and scenes
Stark, S. M., & Stark, C. E. L. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.06.049 · Cited by 132 · see citing works
Staresina, B. P., Michelmann, S., Bonnefond, M., Jensen, O. B., Axmacher, N., & Fell, J. (2016) · eLife · doi:10.7554/elife.17397 · Cited by 122 · see citing works
“Results show that successful associative recognition (AR) yields enhanced event-specific reinstatement of encoding patterns compared to non-associative item recognition (IR).”
BackgroundAging brain mechanics: Progress and promise of magnetic resonance elastography
Hiscox, L. V., Schwarb, H. D., McGarry, M., & Johnson, C. L. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.117889 · Cited by 105 · see citing works
“Importantly, the CA3-DG region has been shown to support the information binding necessary to support relational memory and ensure successful performance in the administered task (Daugherty et al., 2017; Johnston et al., 2016; Rolls, 2016; Yassa & Stark, 2011).”
Mnemonic prediction errors bias hippocampal states
Bein, O., Duncan, K. D., & Davachi, L. (2020) · Nature Communications · doi:10.1038/s41467-020-17287-1 · Cited by 103 · see citing works
“CA3 neurons are highly-interconnected, a feature proposed to facilitate pattern completion and promote the retrieval of encoding related ensembles, which can then be conveyed to area CA1 (Marr, 1971; Montgomery & Buzsaki, 2007; Nakazawa et al., 2002; Norman & O’Reilly, 2003; O’Reilly & McClelland, 1994; Rolls, 2016; T…”
BackgroundHuang, C., Rolls, E. T., Hsu, C. H., Feng, J., & Lin, C. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab113 · Cited by 107 · see citing works
Self-citationRosenbaum, R. S., Kim, A. S. N., & Baker, S. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21037-7 · Cited by 109 · see citing works
Convergence of cortical types and functional motifs in the human mesiotemporal lobe
Paquola, C., Benkarim, O. M., DeKraker, J., Larivière, S., Frässle, S., Royer, J., Tavakol, S., Valk, S. L., Bernasconi, A., Bernasconi, N., et al. (2020) · eLife · doi:10.7554/elife.60673 · Cited by 83 · see citing works
Rolls, E. T. (2022) · Hippocampus · doi:10.1002/hipo.23467 · Cited by 82 · see citing works
“…recognition, and a highly developed eye movement control system to bring the fovea to objects, using mechanisms described elsewhere (Rolls, 2012; Rolls, 2016a; Rolls, 2021a; Rolls, 2021f; Rolls, Aggelopoulos, & Zheng, 2003; Rolls, Deco, et al., 2022b; Rolls, Deco, et al., 2022c; Rolls & Webb,…”
BackgroundMethodInfluentialSelf-citationKent, B. A., Hvoslef‐Eide, M., Saksida, L. M., & Bussey, T. J. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.01.006 · Cited by 81 · see citing works
Daugherty, A. M., Flinn, R., & Ofen, N. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.03.047 · Cited by 77 · see citing works
“In this regard, volumetry of the sub fi elds may be a proxy for cumulative microstructural changes, such as neurogenesis and synaptic pruning — the putative neural basis of associative memory binding and reconstitution (Johnston et al., 2016; Rolls, 2016).”
BackgroundSchemas provide a scaffold for neocortical integration of new memories over time
Audrain, S., & McAndrews, M. P. (2022) · Nature Communications · doi:10.1038/s41467-022-33517-0 · Cited by 76 · see citing works
Fotowat, H., Lee, C., Jun, J. J., & Maler, L. (2019) · eLife · doi:10.7554/elife.44119 · Cited by 69 · see citing works
Stagni, F., Giacomini, A., Guidi, S., Emili, M., Uguagliati, B., Salvalai, M. E., Bortolotto, V., Grilli, M., Rimondini, R., & Bartesaghi, R. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.08.018 · Cited by 63 · see citing works
“Neurogenesis in the hippocampal formation, one of the most important brain regions involved in pattern separation/completion and memory formation (Rolls, 2016), is severely disrupted in fetuses with DS (Contestabile et al.”
Augusto‐Oliveira, M., Arrifano, G. D. P., Malva, J. O., & Lopez, M. E. C. (2019) · Cells · doi:10.3390/cells8020125 · Cited by 61 · see citing works
Spatial Cognition in Teleost Fish: Strategies and Mechanisms
Rodríguez, F., Quintero, B., Amores, L., Madrid, D., Salas-Peña, C., & Salas, C. (2021) · Animals · doi:10.3390/ani11082271 · Cited by 59 · see citing works
Guzman, S. J., Schlögl, A., Espinoza, C., Zhang, X., Suter, B. A., & Jónás, P. (2021) · Nature Computational Science · doi:10.1038/s43588-021-00157-1 · Cited by 58 · see citing works
“(2) To test the effects of temporal structure of the excitatory drive (Supplementary Fig.”
BackgroundMethodInfluentialAnterolateral Entorhinal Cortex Volume Predicted by Altered Intra-Item Configural Processing
Yeung, L., Olsen, R. K., Bild-Enkin, H. E. P., D’Angelo, M. C., Kacollja, A., McQuiggan, D. A., Keshabyan, A., Ryan, J. D., & Barense, M. D. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3664-16.2017 · Cited by 58 · see citing works
“The hippocampus (particularly the trisynaptic loop formed by DG–CA3–CA1) is implicated in pattern separation/completion processes necessary to disambiguate similar stimuli (Norman and O’Reilly, 2003; Rolls, 2016).”
BackgroundElliott, S. B., Harvey‐Girard, E., Giassi, A. C. C., & Maler, L. (2017) · Journal of Comparative Neurology · doi:10.1002/cne.24060 · Cited by 61 · see citing works
Rolls, E. T. (2019) · Hippocampus · doi:10.1002/hipo.23171 · Cited by 52 · see citing works
“This is a decorrelation or orthogonalization process, which is sometimes referred to as pattern separation, and which helps to make the transmission and storage of information have a high capacity (Marr, 1971; McNaughton & Morris, 1987; Rolls, 1987, 1989a, 2016b; Treves & Rolls, 1992).”
BackgroundMethodInfluentialSelf-citationExtensive cortical functional connectivity of the human hippocampal memory system
Ma, Q., Rolls, E. T., Huang, C., Cheng, W., & Feng, J. (2021) · Cortex · doi:10.1016/j.cortex.2021.11.014 · Cited by 50 · see citing works
“…and this is how it is proposed that episodic memory in primates including humans is implemented, for it prototypically involves remembering and later recalling where people or objects have been seen in the spatial environment (Rolls, 2010, 2013a, 2013b, 2016, 2018, 2021a; Kesner & Rolls, 2015).”
BackgroundSelf-citationA theory of hippocampal function: New developments
Rolls, E. T., & Treves, A. (2024) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2024.102636 · Cited by 52 · see citing works
“…effect of diluted connectivity in competitive networks such as the dentate granule cells, because this helps different neurons to fire differently to different inputs even before associative synaptic modification onto high firing rate neurons during the competitive learning (Rolls, 2016a, 2023c).”
BackgroundInfluentialSelf-citationDevelopment of Holistic Episodic Recollection
Ngo, C. T., Horner, A. J., Newcombe, N. S., & Olson, I. R. (2019) · Psychological Science · doi:10.1177/0956797619879441 · Cited by 50 · see citing works
“According to these models, exposure to part of a past experience leads to recurrent connectivity in the hippocampal CA3 subfield, retrieving the conjunctive representation of the entire event (Guzowski, Knierim, & Moser, 2004; Rolls, 2016).”
MethodHardt, O. M., & Nadel, L. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.11.062 · Cited by 49 · see citing works
Event conjunction: How the hippocampus integrates episodic memories across event boundaries
Griffiths, B., & Fuentemilla, L. (2019) · Hippocampus · doi:10.1002/hipo.23161 · Cited by 47 · see citing works
“Pattern separation is thought to accomplish this (e.g., Hunsaker & Kesner, 2013; Rolls, 2010, 2016).”
BackgroundMaurer, A. P., Johnson, S. A., Hernandez, A. R., Reasor, J. E., Cossio, D. M., Fertal, K. E., Mizell, J. M., Lubke, K. N., Clark, B. J., & Burke, S. N. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00049 · Cited by 49 · see citing works
“…a balance between the competing processes of pattern separation and pattern completion within the dentate gyrus-CA3 network (McNaughton and Morris, 1987; Treves and Rolls, 1994; McClelland et al., 1995; O’Reilly and Norman, 2002; Norman and O’Reilly, 2003; Yassa and Stark, 2011; Rolls, 2013, 2015).”
BackgroundOscillatory Reinstatement Enhances Declarative Memory
Javadi, A., Glen, J. C., Halkiopoulos, S., Schulz, M., & Spiers, H. J. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0265-17.2017 · Cited by 47 · see citing works
“This reinstatement may enhance processes such as pattern completion (Staresina et al., 2012, 2016; Tompary et al., 2016) where similar network level inputs are transmitted to regions reconstructing the pattern of activity laid down at encoding, such as is thought to occur in hippocampal area CA3 (Norman and O’Reilly,…”
BackgroundStructure, biophysics, and circuit function of a “giant” cortical presynaptic terminal
Vandael, D., & Jonas, P. (2024) · Science · doi:10.1126/science.adg6757 · Cited by 45 · see citing works
“Classical models of the CA3 circuit suggest that activation of mossy fiber synapses results in the induction of synaptic plasticity in RC CA3-CA3 synapses ( 10 – 12 , 122 ).”
BackgroundInfluentialHippocampal subfields alterations in adolescents with post‐traumatic stress disorder
Postel, C., Viard, A., André, C., Guenolé, F., de Florès, R., Baleyte, J., Gérardin, P., Eustache, F., Dayan, J., & Guillery‐Girard, B. (2018) · Human Brain Mapping · doi:10.1002/hbm.24443 · Cited by 45 · see citing works
“It is widely acknowledged that the hippocampus and its different subfields play a crucial role in memory processes [Horner and Doeller, 2017; Rolls, 2016].”
BackgroundA neural signature of pattern separation in the monkey hippocampus
Sakon, J. J., & SUZUKI, W. A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1900804116 · Cited by 45 · see citing works
“CA3 then becomes the key site of the conflict (1) between encoding of such similar perceptual inputs (pattern separation) and retrieval of stored representations held in the autoassociative network of CA3 via its recurrent collateral circuitry (pattern completion) (2).”
BackgroundHippocampal storage and recall of neocortical “What”–“Where” representations
Rolls, E. T., Zhang, C., & Feng, J. (2024) · Hippocampus · doi:10.1002/hipo.23636 · Cited by 42 · see citing works
Self-citationTransient hippocampal CA1 lesions in humans impair pattern separation performance
Hanert, A., Pedersen, A., & Bartsch, T. (2019) · Hippocampus · doi:10.1002/hipo.23073 · Cited by 44 · see citing works
“…of hippocampal subfields to pattern separation: Computational models assume that the DG performs pattern separation by means of sparse coding of neural activity from the entorhinal cortex (EC) to CA3 thereby decorrelating overlapping neural assemblies (Rolls, 2016; Treves & Rolls, 1994).”
MethodResultSub-second dynamics of theta-gamma coupling in hippocampal CA1
Zhang, L., Lee, J., Rozell, C. J., & Singer, A. C. (2019) · eLife · doi:10.7554/elife.44320 · Cited by 48 · see citing works
“…Moreno et al., 2016; Moser et al., 2017; Moser et al., 2008; O’Keefe, 1976; O’Keefe and Dostrovsky, 1971; O’Keefe and Recce, 1993; Okuyama et al., 2016; Rolls, 2016; Rolls et al., 2005; Rolls and Wirth, 2018; Roy et al., 2017; Sirota and Buzsáki, 2005; Squire et al., 2015; Terrazas, 2005;…”
InfluentialNeurons including hippocampal spatial view cells, and navigation in primates including humans
Rolls, E. T. (2021) · Hippocampus · doi:10.1002/hipo.23324 · Cited by 44 · see citing works
“A key difference is that parts of scenes cannot be moved with respect to other parts of scenes without creating a new spatial scene (Rolls, 2016a; Rolls, 2021).”
BackgroundMethodInfluentialSelf-citationPattern separation and pattern completion: Behaviorally separable processes?
Ngo, C. T., Michelmann, S., Newcombe, N., & Olson, I. R. (2020) · Memory & Cognition · doi:10.3758/s13421-020-01072-y · Cited by 42 · see citing works
“Critically, hippocampal subfields differentially participate in these processes (Montaldi & Mayes, 2010; Neunuebel & Knierim, 2014; O ’ Reilly & McClelland, 1994; Rolls, 2016).”
BackgroundInfluentialCrowley, R., Bendor, D., & Javadi, A. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.04.004 · Cited by 37 · see citing works
“Notably, neural reinstatement depends on the hippocampus because CA3 pyramidal cells have extensive synaptic connections which enable previous patterns of neural activity to be easily reinstated during retrieval (Marr, 1971; Norman & O’Reilly, 2003; Rolls, 2016).”
Hanert, A., Rave, J., Granert, O., Ziegler, M., Pedersen, A., Jan Born, A., Finke, C., & Bartsch, T. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2018.12.046 · Cited by 38 · see citing works
“On a neural level, computational models suggest that within the hippocampal network, the DG performs pattern separation by a decorrelation of overlapping neural assemblies at encoding (Treves and Rolls, 1994; Rolls, 2016).”
InfluentialQuiroga, R. Q. (2023) · Hippocampus · doi:10.1002/hipo.23527 · Cited by 35 · see citing works
Atypical neural topographies underpin dysfunctional pattern separation in temporal lobe epilepsy
Li, Q., Tavakol, S., Royer, J., Larivière, S., de Wael, R. V., Park, B., Paquola, C., Zeng, D., Caldairou, B., Bassett, D. S., et al. (2021) · Brain · doi:10.1093/brain/awab121 · Cited by 38 · see citing works
Hippocampal spatial view cells, place cells, and concept cells: View representations
Rolls, E. T. (2023) · Hippocampus · doi:10.1002/hipo.23536 · Cited by 34 · see citing works
“These analyses emphasize the utility of having a sparse representation in the hippocampus, for sparse distributed representations increase the number of different memories that can be stored (Treves & Rolls, 1991a), essential for an episodic memory (Rolls, 2010, 2016b, 2018, 2023a).”
BackgroundSelf-citationKatsumi, Y., Andreano, J. M., Barrett, L. F., Dickerson, B. C., & Touroutoglou, A. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab157 · Cited by 32 · see citing works
Kraguljac, N. V., Carle, M. S., Frölich, M. A., Tran, S., Yassa, M. A., White, D. M., Reddy, A., & Lahti, A. C. (2017) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2017.02.005 · Cited by 32 · see citing works
RetractedEntorhinal cortex–hippocampal circuit connectivity in health and disease
Hernández‐Frausto, M., & Vivar, C. (2024) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2024.1448791 · Cited by 34 · see citing works
“The DG is thought to contribute to the formation of new episodic memories, novelty, and pattern separation (Bakker et al., 2008; Goodrich-Hunsaker et al., 2008; Rolls, 2016; Leutgeb et al., 2007).”
BackgroundIn Vivo Calcium Imaging of CA3 Pyramidal Neuron Populations in Adult Mouse Hippocampus
Schoenfeld, G., Carta, S., Rupprecht, P., Ayaz, A., & Helmchen, F. (2021) · eNeuro · doi:10.1523/eneuro.0023-21.2021 · Cited by 29 · see citing works
“Neuronal populations in the hippocampal CA3 subfield are part of the mammalian brain circuit 88 that is essential for spatial navigation, memory formation, and cognition (Kesner, 2007; Hartley 89 et al., 2013; Rolls, 2016; Rebola et al., 2017; Hainmueller and Bartos, 2018).”
BackgroundGauffin, H., Landtblom, A., Vigren, P., Frick, A., Engström, M., McAllister, A. M., & Karlsson, T. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2021.746381 · Cited by 30 · see citing works
“A fundamental aspect of many cognitive activities as perception, working memory and LTM, is the ability to discern subtle changes in the environment, often denoted as pattern separation (78).”
BackgroundPishdadian, S., Hoang, N. V., Baker, S., Moscovitch, M., & Rosenbaum, R. S. (2020) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2020.107670 · Cited by 28 · see citing works
Quantitative properties of a feedback circuit predict frequency-dependent pattern separation
Braganza, O., Müller‐Komorowska, D., Kelly, T., & Beck, H. (2020) · eLife · doi:10.7554/elife.53148 · Cited by 26 · see citing works
Neurons as will and representation
Fried, I. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00543-8 · Cited by 27 · see citing works
On pattern separation in the primate, including human, hippocampus
Rolls, E. T. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2021.07.004 · Cited by 25 · see citing works
“25 sparseness of representations in different parts of the human hippocampal system or between the hippocampus and neocortex [1], but in macaques it has been shown that representations in the hippocampus are more sparse than in three neocortical areas [6], in line with the pattern separation hypothesis [3,4].”
ResultSelf-citationCategory specificity in the medial temporal lobe: A systematic review
Robin, J., Rai, Y., Valli, M., & Olsen, R. K. (2018) · Hippocampus · doi:10.1002/hipo.23024 · Cited by 24 · see citing works
Update on temporal lobe‐dependent information processing, in health and disease
Chauvière, L. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14594 · Cited by 25 · see citing works
“LTD mechanisms would need to occur in order to erase some details of older memories (form structured/gist‐ like memories) and fit the network capacity for encoding and recalling (as part of learning) new information (Rolls, 2016, 2017).”
BackgroundDorsal hippocampus is necessary for visual categorization in rats
Kim, J., Castro, L., Wasserman, E. A., & Freeman, J. H. (2018) · Hippocampus · doi:10.1002/hipo.22839 · Cited by 24 · see citing works
“These findings suggest that both category learning and category generalization should depend on the hippocampus (Rolls, 2016).”
BackgroundInfluentialHippocampal circuits underlie improvements in self‐reported anxiety following mindfulness training
Sevinc, G., Greenberg, J., Hölzel, B. K., Gard, T., Calahan, T., Brunsch, V., Hashmi, J. A., Vangel, M. G., Orr, S. P., Milad, M. R., et al. (2020) · Brain and Behavior · doi:10.1002/brb3.1766 · Cited by 23 · see citing works
“…retrieval of extinguished memory is now established (Milad, Wright, et al., 2007), the specific role of subfields is still being investigated (Rolls, 2016); and differential roles have been proposed both in humans (Dimsdale-Zucker, Ritchey, Ekstrom, Yonelinas, & Ranganath, 2018) and in…”
BackgroundBehavioral evidence for pattern separation in human episodic memoryPreprint
Zotow, E., Bisby, J. A., & Burgess, N. (2020) · Learning & Memory · doi:10.1101/lm.051821.120 · Cited by 25 · see citing works
The memory systems of the human brain and generative artificial intelligence
Rolls, E. T. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e31965 · Cited by 23 · see citing works
“The numbers of neurons in different parts of the hippocampal trisynaptic circuit in humans [87] are shown in (a), and indicate very many dentate granule cells, consistent with expansion encoding and the production of sparse uncorrelated representations prior to CA3 [88,89].”
BackgroundSelf-citationLimbic Structures, Emotion, and Memory
Rolls, E. T. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.06857-7 · Cited by 21 · see citing works
“This has many implications for understanding attentional effects to affective value not only on taste, but also on other sensory stimuli (Ge et al., 2012; Luo et al., 2013; Rolls, 2013b, 2014, 2016c).”
BackgroundMethodInfluentialSelf-citationDaugherty, A. M., Schwarb, H. D., McGarry, M., Johnson, C. L., & Cohen, N. J. (2020) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01574 · Cited by 23 · see citing works
“Neurogenesis, dendrization, and pruning within the DG and CA3 are considered to underlie information binding and reconstitution in relational memory (Johnston, Shtrahman, Parylak, Gonçalves, & Gage, 2016; Rolls, 2016).”
BackgroundTranssynaptic modulation of presynaptic short-term plasticity in hippocampal mossy fiber synapses
Vandael, D. H. F., Okamoto, Y., & Jónás, P. (2021) · Nature Communications · doi:10.1038/s41467-021-23153-5 · Cited by 20 · see citing works
Lana, D., Russo, J. D., Mello, T., Wenk, G. L., & Giovannini, M. G. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.11.006 · Cited by 21 · see citing works
“Herewe have demonstrated that themTOR/p70S6Kpathway inCA3pyramidal neurons is activated during the encoding of an inhibitory avoidance memory, confirming the hypothesis that CA3 is especially needed in rapid one trial place memory (Rolls, 2016).”
BackgroundEnriching Hippocampal Memory Function in Older Adults Through Real-World Exploration
Kolarik, B. S., Stark, S. M., Rutledge, S. M., & Stark, C. E. L. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00158 · Cited by 20 · see citing works
“We focused on the MST’s lure discrimination index (LDI), which tests object recognition memory using highly similar lure items in an effort to tax the hippocampal function known as pattern separation (Rolls, 2016; Yassa & Stark, 2011).”
MethodNeural substrates of mnemonic discrimination: A whole‐brain fMRI investigation
Klippenstein, J., Stark, S. M., Stark, C. E. L., & Bennett, I. J. (2020) · Brain and Behavior · doi:10.1002/brb3.1560 · Cited by 20 · see citing works
“…attribute pattern separation to hippocampus (specifically the DG subfield), with limited roles for adjacent medial temporal regions (e.g., memory reinstatement, learning statistical regularities, visual feature extraction; Norman, 2010; O'Reilly, Bhattacharyya, Howard, & Ketz, 2014; Rolls, 2016).”
BackgroundChen, Y.-S., Zhang, S., Yue, C., Xiang, P., Li, J., Wei, Z., Xu, L., & Zeng, Y. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.114033 · Cited by 21 · see citing works
Coppola, V. J., & Bingman, V. P. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.11.019 · Cited by 19 · see citing works
Stress-induced generalization of negative memories is mediated by an extended hippocampal circuit
Ren, L. Y., Meyer, M. A. A., Grayson, V. S., Gao, P., Guedea, A. L., & Radulović, J. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01174-4 · Cited by 19 · see citing works
Sleep shapes the associative structure underlying pattern completion in multielement event memory
Lutz, N. D., Martínez-Albert, E., Friedrich, H., Jan Born, A., & Besedovsky, L. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2314423121 · Cited by 19 · see citing works
“32 ).”
Daugherty, A. M., Sutton, B. P., Hillman, C. H., Kramer, A. F., Cohen, N. J., & Barbey, A. K. (2019) · Trends in Neuroscience and Education · doi:10.1016/j.tine.2019.100123 · Cited by 19 · see citing works
Age-related differences in encoding-retrieval similarity and their relationship to false memory
Chamberlain, J. D., Bowman, C. R., & Dennis, N. A. (2022) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2022.01.011 · Cited by 19 · see citing works
Katsumi, Y., Kamona, N., Zhang, J., Bunce, J. G., Hutchinson, J. B., Yarossi, M., Tunik, E., Quigley, K. S., Dickerson, B. C., & Barrett, L. F. (2021) · doi:10.1101/2021.09.01.456844 · Cited by 89 · see citing works
Experience-Dependent Effects of Muscimol-Induced Hippocampal Excitation on Mnemonic Discrimination
Johnson, S. A., Turner, S. M., Lubke, K. N., Cooper, T. L., Fertal, K. E., Bizon, J. L., Maurer, A. P., & Burke, S. N. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2018.00072 · Cited by 18 · see citing works
“…orthogonalization of inputs from parahippocampal cortical regions, minimizing interference (McNaughton and Morris, 1987; Treves and Rolls, 1992; O’Reilly and McClelland, 1994; Rolls and Kesner, 2006; Treves et al., 2008; Yassa and Stark, 2011; Santoro, 2013; Kesner and Rolls, 2015; Rolls, 2016).”
BackgroundNitschke, J. P., Giorgio, L.-M., Zaborowska, O., & Sheldon, S. (2020) · Stress · doi:10.1080/10253890.2020.1724946 · Cited by 17 · see citing works
“…Montreal, Canada, H3A 1G1 2020 Informa UK Limited, trading as Taylor & Francis Group been linked to the functioning of the dentate gyrus of the hippocampus (Rolls, 2016), which is a hippocampal subfield that is particularly sensitive to the effects of acute stress (McEwen, Nasca, & Gray, 2016).”
BackgroundXie, W., Cappiello, M., Yassa, M. A., Ester, E. F., Zaghloul, K. A., & Zhang, W. (2023) · eLife · doi:10.7554/elife.83365 · Cited by 20 · see citing works
Świetlik, D., Białowas, J., Kusiak, A., & Cichońska, D. (2018) · Folia Morphologica · doi:10.5603/fm.a2018.0042 · Cited by 16 · see citing works
On the novel mechanisms for social memory and the emerging role of neurogenesis
Lunardi, P. S., Mansk, L. M. Z., Jaimes, L. F., & Pereira, G. S. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.03.006 · Cited by 16 · see citing works
Low-Resolution Neurocognitive Aging and Cognition: An Embodied Perspective
Mille, J., Brambati, S. M., Izaute, M., & Vallet, G. T. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.687393 · Cited by 16 · see citing works
Remembering rewarding futures: A simulation‐selection model of the hippocampus
Jung, M. W., Lee, H., Jeong, Y., Lee, J. W., & Lee, I. (2018) · Hippocampus · doi:10.1002/hipo.23023 · Cited by 15 · see citing works
“…1999; Hasselmo & Wyble, 1997; Lever et al., 2010; Levy, 1989; Lisman & Otmakhova, 2001; Vago & Kesner, 2008), pattern completion (Cheng, 2013; Rolls, 2016), processing temporal information (Gilbert et al., 2001; Mankin et al., 2012; Rolls & Kesner, 2006), transforming CA3 representations for…”
Rolls, E. T. (2024) · Hippocampus · doi:10.1002/hipo.23666 · Cited by 17 · see citing works
Self-citationRolls, E. T., & Kesner, R. P. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.02.001 · Cited by 14 · see citing works
“Pattern completion is an inherent property of an autoassociation or attractor network such as the CA3 recurrent collateral system is believed to be (Rolls, 2008, 2016a), and there is also therefore great interest in the mechanisms for pattern completion in the hippocampal system.”
BackgroundInfluentialSelf-citationPoor Mnemonic Discrimination Predicts Overgeneralization of Fear
Bernstein, E. E., van der Does, F. H. S., Orr, S. P., & McNally, R. J. (2020) · Journal of Psychopathology and Behavioral Assessment · doi:10.1007/s10862-020-09846-z · Cited by 13 · see citing works
Buchberger, E. S., Ngo, C. T., Peikert, A., Brandmaier, A. M., & Werkle‐Bergner, M. (2024) · Behavior Research Methods · doi:10.3758/s13428-024-02396-2 · Cited by 12 · see citing works
“Important to learning specific episodes are pattern separation that discriminates between similar memories through the reduction of representational similarity, and pattern completion that retrieves linked associations among co-occurring elements (Marr, 1971; Norman & O’Reilly, 2003; Rolls, 2016).”
BackgroundKraguljac, N. V., Carle, M. S., Frölich, M. A., Tran, S., Yassa, M. A., White, D. M., Reddy, A., & Lahti, A. C. (2021) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.09.008 · Cited by 12 · see citing works
He, M., Li, Y., Zhou, L., Li, Y., Lei, T., Yan, W., Song, J., & Chen, L. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.823535 · Cited by 13 · see citing works
“…the left and right hippocampus was detected, as well as functional lateralization; for example, the right hippocampus may be devoted to episodic memories with spatial and visual components, whereas the left hippocampus may be devoted to memories with verbal or linguistic components (Rolls, 2016).”
MethodKim, S., & Lim, W. (2022) · Physical review. E · doi:10.1103/physreve.105.014418 · Cited by 12 · see citing works
Rolls, E. T. (2021) · Brain Structure and Function · doi:10.1007/s00429-021-02347-z · Cited by 12 · see citing works
“Given that there is one principal excitatory neuron type in the neocortex, the pyramidal cell (Rolls 2016a), the research described here is conceptually an important advance, for it shows that all these types of computation can be performed with one type of single neuron with the connections and…”
BackgroundMethodInfluentialSelf-citationPattern separation of fear extinction memoryPreprint
Laing, P. A. F., & Dunsmoor, J. E. (2023) · Learning & Memory · doi:10.1101/lm.053760.123 · Cited by 13 · see citing works
“…items bothshowedenhancedrecognition(CS + >CS − )butdivergedaccord-ing to the canonical memory systems of “ pattern completion ” and “ pattern separation, ” which are well documented across decades of memory research (Marr 1971; Rolls 2016) yet rarely studied in the context of human fear memory.”
BackgroundNeuropathology of a remarkable case of memory impairment informs human memory
Gao, A. F., Keith, J. L., Gao, F., Black, S. E., Moscovitch, M., & Rosenbaum, R. S. (2020) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2020.107342 · Cited by 11 · see citing works
Flexible communication between cell assemblies and ‘reader’ neuronsPreprint
Pompili, M. N., Todorova, R., Boucly, C. J., Leroux, E. M., Wiener, S. I., & Zugaro, M. B. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.06.506754 · Cited by 11 · see citing works
“Two generic computations of funda-147 mental theoretical relevance ( 37 ) are pattern completion, which allows accurate retrieval or generalization from partial inputs, and pattern separation, which improves discrimination of similar inputs ( 4,35,37,44 ).”
BackgroundInfluentialMismatch negativity as a marker of auditory pattern separation
Herman, D., Baker, S., Chow, R., Cazes, J., Alain, C., & Rosenbaum, R. S. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad274 · Cited by 10 · see citing works
Hippocampal Engrams and Contextual Memory
Vasudevan, K., Hassell, J. E., & Maren, S. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-62983-9_4 · Cited by 10 · see citing works
Kim, S.-Y., & Lim, W. (2022) · Cognitive Neurodynamics · doi:10.1007/s11571-022-09797-z · Cited by 10 · see citing works
“As a preprocessor for the CA3, the principal GCs perform pattern separation on the input patterns from the EC by sparsifying and orthogonalizing them, and send the pattern-separated outputs to the pyramidal cells in the CA3 through the mossy fibers (MFs) (Treves and Rolls 1994; O’Reilly and McClelland 1994; Schmidt et…”
BackgroundMethodTheta-phase-specific modulation of dentate gyrus memory neurons
Rahsepar, B., Noueihed, J., Norman, J. F., Lahner, B., Quick, M. H., Ghaemi, K., Pandya, A., Fernandez, F. R., Ramirez, S., & White, J. A. (2023) · eLife · doi:10.7554/elife.82697 · Cited by 10 · see citing works
- Authors
- Rolls, E. T.
- Affiliations
- University of Warwick (GB)
- Corresponding author
- Rolls, Edmund T.
- ORCID
- Rolls, Edmund T.
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2016-03
- Volume
- 129
- Pages
- 4-28
- ISSN
- 1074-7427 (ISSN-L)
- OpenAlex
- W889908523
- Semantic Scholar
- dee8fed2414a8b21d9bf5724732f82ca2356190b
- Cited by
- 234
- References
- 227
- Citations by year
- 2026: 28 · 2025: 25 · 2024: 29 · 2023: 24 · 2022: 19 · 2021: 29 · 2020: 18 · 2019: 21 · 2018: 17 · 2017: 15 · 2016: 9
- FWCI
- 8.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurobiology of Learning and Memory (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Medical Research Council
- Human Frontier Science Program
- EEC BRAIN
- MRC Oxford Interdisciplinary Research Centre in Cognitive Neuroscience
- Oxford McDonnell-Pew Centre in Cognitive Neuroscience
- Oxford Centre for Computational Neuroscience
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- pattern separation, pattern completion, hippocampus, CA3, dentate gyrus, neocortex, attractor networks, sparse distributed representations, mossy fibers, long-term potentiation, perforant path, entorhinal cortex, place cells, grid cells, competitive learning, pattern generalization, memory retrieval
- MeSH terms
- Animals, Association Learning, Humans, Models, Neurological, Neural Pathways, Neurons, Mental Recall, Synapses, Neocortex, Pattern Recognition, Physiological, CA3 Region, Hippocampal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
